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Unveiling Microbial Activities Along the Halocline of Thetis, a Deep-Sea Hypersaline Anoxic Basin

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Unveiling Microbial Activities Along the Halocline of Thetis, a Deep-Sea Hypersaline Anoxic Basin The ISME Journal (2014) 8, 2478–2489 & 2014 International Society for Microbial Ecology All rights reserved 1751-7362/14 www.nature.com/ismej ORIGINAL ARTICLE Unveiling microbial activities along the halocline of Thetis, a deep-sea hypersaline anoxic basin Maria G Pachiadaki1, Michail M Yakimov2, Violetta LaCono2, Edward Leadbetter1 and Virginia Edgcomb1 1Woods Hole Oceanographic Institution, Woods Hole, MA, USA and 2CNR–Institute for Coastal Marine Environment, Messina, Italy Deep-sea hypersaline anoxic basins (DHABs) in the Eastern Mediterranean Sea are considered some of the most hostile environments on Earth. Little is known about the biochemical adaptations of microorganisms living in these habitats. This first metatranscriptome analysis of DHAB samples provides significant insights into shifts in metabolic activities of microorganisms as physicochem- ical conditions change from deep Mediterranean sea water to brine. The analysis of Thetis DHAB interface indicates that sulfate reduction occurs in both the upper (7.0–16.3% salinity) and lower (21.4–27.6%) halocline, but that expression of dissimilatory sulfate reductase is reduced in the more hypersaline lower halocline. High dark-carbon assimilation rates in the upper interface coincided with high abundance of transcripts for ribulose 1,5-bisphosphate carboxylase affiliated to sulfur- oxidizing bacteria. In the lower interface, increased expression of genes associated with methane metabolism and osmoregulation is noted. In addition, in this layer, nitrogenase transcripts affiliated to uncultivated putative methanotrophic archaea were detected, implying nitrogen fixation in this anoxic habitat, and providing evidence of linked carbon, nitrogen and sulfur cycles. The ISME Journal (2014) 8, 2478–2489; doi:10.1038/ismej.2014.100; published online 20 June 2014 Introduction extreme salinities (high densities) of DHABs act as a barrier to seawater mixing and salt diffusion, Microorganisms exhibit an incredible diversity of physically isolating them from other marine habi- physiologies and behaviors that allow them to tats, selecting for organisms adapted to multiple exploit virtually all habitats on our planet. These ‘stressors’ and probably preventing dispersal of habitats include many that seemed uninhabitable, those organisms. An interface layer, with a sharp such as those characterized by physicochemical oxycline, redoxcline and halocline, separates the parameters with values close to the limits known hypersaline brine body and the oxygenated sea to support life. Deep-sea hypersaline anoxic basins water. (DHABs) are considered to be some of the most Thus far, DHABs in the Mediterranean and Red hostile environments because of their combination Sea have provided exciting new insights into novel of extreme physicochemical features, including microbial diversity and have extended our know- nearly saturated salt concentration and correspond- ledge of environmental factors that define the limits ing low water activity, high hydrostatic pressure, of life (Eder et al., 1999, 2001; Hallsworth et al., anoxia and high sulfide concentration. Typical 2007). Studies of Discovery, L’Atalante, Urania, DHABs of Eastern Mediterranean are 43000 m Thetis and Bannock basins revealed that DHAB below sea level; their origin is associated with the interfaces harbor abundant and diverse microbial Miocene Messinian salinity crisis 5.59–5.33 million communities that include numerous novel candi- years ago. The genesis of the brine bodies on the sea date divisions that are more productive than most floor of the Eastern Mediterranean Sea occurred pelagic marine systems (see, for example, Sass et al., 2000–176 000 years ago through either the de novo 2001; Van Der Wielen et al., 2005; Yakimov et al., dissolution of buried Messinian evaporitic deposits 2007; Edgcomb et al., 2009; Stock et al., 2012). or the ejection into seafloor depressions of ancient Functional analyses of these communities based on interstitial evaporated sea water entrapped in those PCR amplification of key functional genes as well as deposits (Cita, 2006 and references therein). The activity measurements revealed sulfur cycling and methanogenesis to be dominant prokaryotic meta- Correspondence: MG Pachiadaki or V Edgcomb, Woods Hole bolic processes supporting life in DHABs and Oceanographic Institution, 266 Woods Hole Road, MS #8, 02543 contributing to observed elevated biomass in DHAB Woods Hole, MA, USA. haloclines (Daffonchio et al., 2006; Yakimov et al., E-mail: [email protected] or [email protected] Received 4 February 2014; revised 30 April 2014; accepted 11 2007; Borin et al., 2009). Recent advances in May 2014; published online 20 June 2014 RNA isolation, amplification and high-throughput Metatranscriptomics analysis of Thetis interface MG Pachiadaki et al 2479 sequencing make it possible to acquire millions of depths was carried out using the Winkler method sequences of transcribed genes from microbial with an automatic end point detection burette (716 communities. Metatranscriptomics is a powerful DNS Titrino, Metrohm AG, Herisau, Switzerland). tool for examining microbial community activities Water from two distinct horizons (each representing that enables inferences about the relative expression a distinct range of salinity and oxygen between the of diverse metabolic pathways based upon tran- top and bottom of each Niskin bottle) was collected script abundance as a proxy for gene expression from the Thetis interface; the upper interface (UI) (Frias-Lopez et al., 2008; Stewart et al., 2011). layer corresponding to 7.0–16.3% salinity, and the Thetis, discovered in 2008, is among the best- lower (LI) layer with 21.4–27.6% salinity. Oxygen in studied deep-sea hypersaline basins. Chemical the UI sample ranged from 9.5 mmol l À 1 to undetect- analysis of the brine body shows it is almost nine able, and remained undetectable in the lower times more saline than sea water, with an ion sample. From each horizon, ca. 12 l of water was composition reflecting late-stage evaporites. Based collected on Durapore membranes (47 mm, 0.65 mm, on this, the Thetis brine is argued to originate Millipore, Millford, MA, USA) under gentle pres- from ancient trapped interstitial brines rather sure (B100 ml min À 1), using a peristaltic pump than dissolution of halite (La Cono et al., 2011). (Ecoline ISM 1079, Ismatec, Germany). The filters A pronounced stratification of both prokaryotic and were stored in RNA Shield (Zymo Research, Orange, eukaryotic communities was observed over the CA, USA) at À 80 1C until analysis. B2 m thick interface, as was a distinction between halocline and brine communities (La Cono et al., RNA extractions 2011; Stock et al., 2012). A recent metagenomics Two replicate RNA extractions were processed per study of the Thetis brine and halocline (Ferrer et al., depth representing a total of 12 l of water per 2012) provided increased understanding of the horizon studied. The liquid RNA Shield and the metabolic potential of microbial communities of filters were extracted separately. The RNA Shield these habitats. However, [14 C]-bicarbonate assimila- was transferred to 50 ml tubes and centrifuged at tion rates and reverse transcriptase-PCR of a few 4000 g for 3 min to remove particulates. An equal functional genes in samples from the same Thetis volume of 100% ethanol was added to the super- habitats detected activities not suggested by the natant, mixed, transferred to an RNeasy Midi Kit metagenome (La Cono et al., 2011), including the (Qiagen, Hildesheim, Germany) column and pro- expression of ribulose 1,5-bisphosphate carboxy- cessed following the manufacturer’s recommenda- lase. Such inconsistency points to the need for tions. Contaminating DNA was removed by TURBO metatranscriptomic information on a wider range of DNAse treatment (Life Technologies, Grand Island, metabolic activities for a better understanding of NY, USA) according to the manufacturer’s instruc- community processes. tions. Total RNA was purified with the MEGA Clear To elucidate active metabolic pathways of micro- Kit (Life Technologies) as directed and suspended in organisms in the Thetis interface, we applied whole 100 mldH2O. community metatranscriptomics to samples from The filters were transferred into Lysing Matrix E two distinct positions along the halocline that differ tubes (MP Biomedicals, Solon, OH, USA). Then, in salinity and oxygen concentration. This study 4 ml of RNeasy Midi Kit Buffer RTL (Qiagen) was presents the first transcriptome analysis of micro- added, homogenized for 60 s at 4.0 m s À 1 using a biota from a DHAB halocline, and provides the first FastPrep-24 (MP Biomedicals) and centrifuged for insights of expressed genes other than ribosomal 10 min at 4000 g. Liquids were transferred to clean RNA from the eukaryotic microbial community. tubes, 1 volume of 70% ethanol was added to each tube and extracts were processed following the RNeasy kit instructions. Extractions were treated Materials and methods with DNase and purified with the MEGA Clear kit as described above. Fluid and filter extracts were Sampling of Thetis halocline combined for each sample and concentrated by Sampling of Thetis (341 40.158 N, 221 08.703 E) was ethanol precipitation. Absence of DNA was con- conducted from the R/V Urania on 20 September firmed by 40 cycles of PCR using the general 2012. The seawater/brine interface of Thetis is at a bacterial small subunit ribosomal RNA (SSU rRNA) depth of 3258 m below sea level and the brine gene primer 8F and
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